Microbial landscapes in Trinervitermes trinervoides termite colonies are affected by mound compartments and soil properties but not by symbiotic Podaxis fungi

Abstract

Termites are important ecosystem engineers and play key roles in modulating microbial communities within and outside their mounds. Microbial diversity within termite mounds is generally lower than surrounding soils, due to termite-associated antimicrobial compounds and active sanitary behaviours. Microbial symbionts of termites can also influence the microbial landscape, by inhibiting or out-competing other microbes. Certain members of the arid habitat fungal genus Podaxis (Agaricomycetes; Agaricaceae) are symbiotic with savannah specialist grass-cutting termites, and have the potential to influence mound-associated microbiomes. To test this, we characterized fungal (ITS2) and bacterial (16S rRNA) communities within and outside 49 Trinervitermes trinervoides mounds with and without Podaxis fruiting bodies across a 1000 km transect in South Africa. We predicted that Podaxis would be a dominant member of the fungal communities in mounds and negatively impact microbial diversity. Further, we explored how environmental variables shaped microbial communities, including whether soil elemental composition affected Podaxis presence. As expected, we observed less diverse fungal communities, but not bacterial communities, within than outside mounds, while microbial communities differed by sampling regions and mound compartments. Podaxis sequences were present in 48 out of 49 mounds in low relative abundances, and neither fruiting body presence nor sequence abundance were associated with microbial diversity or composition. There was, however, an overall association between the presence of Podaxis fruiting bodies and elemental composition, with different elements displaying varying associations depending on geographic region. Both environmental variables and soil elements were associated with fungal and bacterial taxa, indicating that they are key drivers of microbial community composition. Taken together, our findings suggest that microbial landscapes in termite mounds are not strongly influenced by Podaxis but mainly driven by termite filtering and regional abiotic variables and elemental compositions.

Description

DATA AVAILABILITY : Fungal (PRJNA1100193) and bacterial (PRJNA1100180) amplicon sequences are available from the SRA Archive in GenBank. Termite COI sequences can be found in Table S1. Original datasets and R scripts used for microbiome analyses can be found in Zenodo online repository: https://doi.org/10.5281/zenodo.13895044.

Keywords

Podaxis, MiSeq amplicon sequencing, Symbioses, Termites, Microbial communities

Sustainable Development Goals

SDG-15: Life on land

Citation

Bodawatta, K.H., Maccario, L., Peereboom, N. et al. 2024, 'Microbial landscapes in trinervitermes trinervoides termite colonies are affected by mound compartments and soil properties but not by symbiotic Podaxis fungi', Science of the Total Environment, vol. 957, art. 177015, pp. 1-13. https://doi.org/10.1016/j.scitotenv.2024.177015.